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Specificity of Herbivore-Induced Hormonal Signaling and Defensive Traits in Five Closely Related Milkweeds (Asclepias Spp.) Auth

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Specificity of Herbivore-Induced Hormonal Signaling and Defensive Traits in Five Closely Related Milkweeds (Asclepias Spp.) Auth Author's personal copy J Chem Ecol (2014) 40:717–729 DOI 10.1007/s10886-014-0449-6 Specificity of Herbivore-Induced Hormonal Signaling and Defensive Traits in Five Closely Related Milkweeds (Asclepias spp.) Anurag A. Agrawal & Amy P. Hastings & Eamonn T. Patrick & Anna C. Knight Received: 5 December 2013 /Revised: 23 April 2014 /Accepted: 6 May 2014 /Published online: 27 May 2014 # Springer Science+Business Media New York 2014 Abstract Despite the recognition that phytohormonal signal- associated with endogenous JA levels, even among low-latex ing mediates induced responses to herbivory, we still have species; 2) correlations among milkweed hormones are gen- little understanding of how such signaling varies among close- erally positive, although herbivore damage induces a diver- ly related species and may generate herbivore-specific in- gence (tradeoff) between JA and SA; 3) induction of duced responses. We studied closely related milkweeds cardenolides and latex are not necessarily physiologically (Asclepias) to link: 1) plant damage by two specialist chewing linked; and 4) even very closely related species show highly herbivores (milkweed leaf beetles Labidomera clivicolis and divergent induction, with some species showing strong de- monarch caterpillars Danaus plexippus); 2) production of the fenses, hormonally-mediated induction, and impacts on her- phytohormones jasmonic acid (JA), salicylic acid (SA), and bivores, while other milkweed species apparently use alterna- abscisic acid (ABA); 3) induction of defensive cardenolides tive strategies to cope with insect attack. and latex; and 4) impacts on Danaus caterpillars. We first show that A. syriaca exhibits induced resistance following Keywords Cardenolides . Coevolution . Common milkweed monarch herbivory (i.e., reduced monarch growth on previ- Asclepias syriaca . Jasmonic acid . Latex . Monarch butterfly ously damaged plants), while the defensively dissimilar Danaus plexippus . Phytohormones . Plant-insect interactions A. tuberosa does not. We next worked with a broader group of five Asclepias, including these two species, that are highly divergent in defensive traits yet from the same clade. Three of Introduction the five species showed herbivore-induced changes in cardenolides, while induced latex was found in four species. Understanding how plants use phenotypic plasticity to re- Among the phytohormones, JA and ABA showed specific spond to diverse environmental cues has been a long- responses (although they generally increased) to insect species standing question in plant evolutionary ecology (Agrawal and among the plant species. In contrast, SA responses were 2001). It generally is assumed that, given the lack of a nervous consistent among plant and herbivore species, showing a system, plant hormonal responses orchestrate myriad plant decline following herbivore attack. Jasmonic acid showed a responses, including defense induction to specific herbivores. positive quantitative relationship only with latex, and this was Even so, with only a handful of phytohormones, they must strongest in plants damaged by D. plexippus. Although phy- function together or in particular ratios to dictate distinct tohormones showed qualitative tradeoffs (i.e., treatments that responses (Reymond and Farmer 1998). In particular, the enhanced JA reduced SA), the few significant individual intersection of multiple hormones has played a critical role plant-level correlations among hormones were positive, and in understanding plant responses to important biotic and abi- these were strongest between JA and ABA in monarch dam- otic interactions such as herbivory, microbial attack, light aged plants. We conclude that: 1) latex exudation is positively competition, and water stress (Cipollini 2004;Morenoetal. 2009; Thaler and Bostock 2004; von Dahl and Baldwin 2007). * : : : A. A. Agrawal ( ) A. P. Hastings E. T. Patrick A. C. Knight For plant responses to insect attack, jasmonic acid (JA) is Department of Ecology and Evolutionary Biology, and Department of Entomology, Cornell University, Ithaca, NY, USA recognized as the master regulator of induced defense, espe- e-mail: [email protected] cially against chewing herbivores (Agrawal 2011; Erb et al. Author's personal copy 718 J Chem Ecol (2014) 40:717–729 2009, 2012; Halitschke and Baldwin 2003). Despite playing a role in a few other known plant functions (Avanci et al. 2010), jasmonates are nearly universally upregulated following chewing damage, and are known to play a key role in cueing a remarkably diverse set of plant defenses spanning toxins and trichomes to volatiles and extrafloral nectar (Erb et al. 2009; Halitschke and Baldwin 2003;Heiletal.2004; Rasmann et al. 2009;Thaleretal.2002;TrawandBergelson2003). Nonetheless, it is clear that other plant hormones, namely salicylic acid (SA), abscisic acid (ABA), and ethylene (ET) play roles as antagonists and synergists in defensive reactions (Erb et al. 2012;Thaleretal.2012). Thus, the simultaneous examination of multiple phytohormones during plant defen- sive responses has been advocated as an approach to under- standing specificity in plant-herbivore interactions (Schmelz et al. 2003; Schuman et al. 2009; Thaler et al. 2010). Our approach to unraveling specificity of plant responses to herbivory in this study was two-fold. First, we chose to work within a guild of specialized chewing herbivores (a coleopteran, the milkweed leaf beetle Labidomera clivicolis and a lepidopteran, the monarch butterfly Danaus plexippus), native to a wild system (the milkweeds), and sharing a long evolutionary history. The fact that the herbivores are within Fig. 1 Phylogenetic relationships within a monophyletic clade of the same guild allows for inferences about specificity in Asclepias (Apocynaceae). Shown are all of the extant species in this induced responses that go beyond the impacts of different clade. Relationships are based on a recent molecular phylogeny (Fishbein feeding styles. Second, we worked with a set of closely related et al. 2011). Arrows and plant images indicate the species studied here. host plant species, with known phylogenetic relationships. Based on previous work, the five studied species fall among three distinct plant defense syndromes (Agrawal and Fishbein 2006). Photo credits Thus, we addressed how very closely related species have from top to bottom are: Mark Fishbien, Marc Johnson, AAA, AAA, diverged in their physiological processes, and whether this has and Ellen Woods resulted in divergent specificity in plant-herbivore relation- ships. Although such an approach has the drawback of re- Accordingly, we asked the following questions: 1) Do two duced mechanistic detail compared to a single plant-herbivore phenotypically divergent, but closely related and sympatric association, we are seeking to make broad evolutionary infer- Asclepias species differ in the extent to which they exhibit ences about how defense specificity can evolve. induced resistance to monarch caterpillars? 2) How variable In particular, we have been studying North American are five closely related Asclepias species in their induced plant Asclepias spp. (Apocynaceae), which are a monophyletic responses (cardenolides and latex) when attacked by different genus comprising approximately 140 species in the Western specialist chewing herbivores? 3) To what extent are plant Hemisphere (Agrawal et al. 2009; Fishbein et al. 2011; hormones (JA, SA, and ABA) linked to the induced re- Woodson 1954). Here, we focused on 5 species in a mono- sponses? and, 4) Are the relationships between plant hor- phyletic clade consisting of 9 total taxa (Fig. 1), including the mones dependent on plant species and the biotic context common milkweed A. syriaca, which is the best studied (i.e., damage by different herbivore species)? In summary, species for interactions between monarch butterflies and plant our goal was to develop a predictive framework for how defense (Bingham and Agrawal 2010; Malcolm et al. 1989; different herbivores induce specific plant defensive responses, Malcolm and Zalucki 1996; Van Zandt and Agrawal 2004b; and to employ a comparative approach to address how such Vannette and Hunter 2011). Because all species produce two induced responses have evolved. potent defenses, latex and cardenolides, neither of which has a credibly hypothesized function other than defense, we have an excellent model system to address specificity in the context of evolutionarily relevant interactions (Agrawal and Konno Methods and Materials 2009; Ali and Agrawal 2012). Furthermore, these species are known to have overall divergences in their defensive Plant Growth and Herbivores All plants were germinated strategies, making the comparisons highly informative from wild-collected seed in petri dishes containing moist (Agrawal and Fishbein 2006; Agrawal et al. 2009). paper towels, transplanted into 500 ml plastic pots with Pro- Author's personal copy J Chem Ecol (2014) 40:717–729 719 Mix BX soil, and fertilized twice with a dilute fertilizer (NPK N was 5 in the A. obovata–Labidomera combination). 21:5:20, 150 ppm N). We fully randomized the plants (one per Labidomera is oligophagous, known to eat many Asclepias pot) in growth chambers (400 μmoles/m2/sec light, 14/8 h L/D spp. In all cases, young larvae (second and third instars were cycle, 28 °C/24 °C temperature cycle), intermixing all plants used to damage plants). Insects were maintained on the from a given experiment in a single chamber. Plants were plants in mesh cages; after three full
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